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RLK7, a leucine-rich repeat receptor-like kinase, is required for proper germination speed and tolerance to oxidative stress in Arabidopsis thaliana

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Abstract

The leucine-rich repeat class of receptor-like kinase (LRR-RLKs) encoding genes represents the largest family of putative receptor genes in the Arabidopsis thaliana genome. However, very little is known about the range of biological process that they control. We present in this paper the functional characterization of RLK7 that has all the structural features of a receptor-like kinase of the plant-specific LRR type. To this end, we identified and characterized three independent T-DNA insertion mutants, constructed lines carrying truncated versions of this putative receptor, one lacking the cytoplasmic kinase domain (RLK7Δkin) and the other one lacking 14 LRR repeats (RLK7ΔLRR) and generated RLK7 overexpressing lines. We thus provide evidences that RLK7 is involved in the control of germination speed and the tolerance to oxidant stress. First, consistent with the expression kinetics of the RLK7 gene in the seeds, we found that all three mutants showed a delay in germination, whereas the overexpressors, RLK7Δkin and RLK7ΔLRR lines displayed a phenotype of more precocious germination. Second, a non-hypothesis driven proteomic approach revealed that in the seedlings of the three T-DNA insertion lines, four enzymes directly or indirectly involved in reactive oxygen species detoxification, were significantly less abundant. Consistent with this finding, the three mutants were less tolerant than the wild type to a hydrogen peroxide treatment, whereas the overexpressors, RLK7Δkin and RLK7ΔLRR lines presented the opposite phenotype.

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Abbreviations

LRR:

Leucine-rich repeat

RLK:

Receptor-like kinase

ABA:

Abscisic acid

GA:

Gibberellins

ABI3:

ABSCISIC ACID INSENSITIVE3

FUS3:

FUSCA3

LEC1:

LEAFY COTYLEDON1

ROS:

Reactive oxygen species

GUS:

β-Glucuronidase

2-D DIGE:

Two-dimensional differential in gel electrophoresis

References

  • Afzal AJ, Wood AJ, Lightfoot DA (2008) Plant receptor-like serine threonine kinases: roles in signaling and plant defense. Mol Plant Microbe Interact 21:507–517

    Article  CAS  PubMed  Google Scholar 

  • Albrecht C, Russinova E, Hecht V, Baaijens E, de Vries S (2005) The Arabidopsis thaliana SOMATIC EMBRYOGENESIS RECEPTOR-LIKE KINASES1 and 2 control male sporogenesis. Plant Cell 17:3337–3349

    Article  CAS  PubMed  Google Scholar 

  • Alonso JM, Stepanova AN, Leisse TJ, Kim CJ, Chen H, Shinn P, Stevenson DK, Zimmerman J, Barajas P, Cheuk R, Gadrinab C, Heller C, Jeske A, Koesema E, Meyers CC, Parker H, Prednis L, Ansari Y, Choy N, Deen H, Geralt M, Hazari N, Hom E, Karnes M, Mulholland C, Ndubaku R, Schmidt I, Guzman P, Aguilar-Henonin L, Schmid M, Weigel D, Carter DE, Marchand T, Risseeuw E, Brogden D, Zeko A, Crosby WL, Berry CC, Ecker JR (2003) Genome-wide insertional mutagenesis of Arabidopsis thaliana. Science 301:653–657

    Article  PubMed  Google Scholar 

  • Bailly C (2004) Active oxygen species and antioxidants in seed biology. Seed Sci Res 14:93–107

    Article  CAS  Google Scholar 

  • Bailly C, El-Maarouf-Bouteau H, Corbineau F (2008) From intracellular signaling networks to cell death: the dual role of reactive oxygen species in seed physiology. CR Biol 331:806–814

    Article  CAS  Google Scholar 

  • Becraft PW (2002) Receptor kinase signaling in plant development. Annu Rev Cell Dev Biol 18:163–192

    Article  CAS  PubMed  Google Scholar 

  • Bentsink L, Koornneef M (2009) Seed dormancy and germination. In: Last R, Chang C, Jander G, Kliebenstein D, McClung R, Millar H (eds) The Arabidopsis book. The American Society of Plant Biologists, Rockville, MD, pp 1–18

    Google Scholar 

  • Bewley JD (1997) Seed germination and dormancy. Plant Cell 9:1055–1066

    Article  CAS  PubMed  Google Scholar 

  • Boller T, Felix G (2009) A renaissance of elicitors: perception of microbe-associated molecular patterns and danger signals by pattern-recognition receptors. Annu Rev Plant Biol 60:379–406

    Article  CAS  PubMed  Google Scholar 

  • Braun DM, Walker JC (1996) Plant transmembrane receptors: new pieces in the signaling puzzle. Trends Biochem Sci 21:70–73

    CAS  PubMed  Google Scholar 

  • Carles C, Bies-Etheve N, Aspart L, Leon-Kloosterziel KM, Koornneef M, Echeverria M, Delseny M (2002) Regulation of Arabidopsis thaliana Em genes: role of ABI5. Plant J 30:373–383

    Article  CAS  PubMed  Google Scholar 

  • Chinchilla D, Shan L, He P, de Vries S, Kemmerling B (2009) One for all: the receptor-associated kinase BAK1. Trends Plant Sci 14:535–541

    Article  CAS  PubMed  Google Scholar 

  • Cho SK, Larue CT, Chevalier D, Wang H, Jinn TL, Zhang S, Walker JC (2008) Regulation of floral organ abscission in Arabidopsis thaliana. Proc Natl Acad Sci USA 105:15629–15634

    Article  CAS  PubMed  Google Scholar 

  • Clerkx EJ, El-Lithy ME, Vierling E, Ruys GJ, Blankestijn-De Vries H, Groot SP, Vreugdenhil D, Koornneef M (2004) Analysis of natural allelic variation of Arabidopsis seed germination and seed longevity traits between the accessions Landsberg erecta and Shakdara, using a new recombinant inbred line population. Plant Physiol 135:432–443

    Article  CAS  PubMed  Google Scholar 

  • Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16:735–743

    Article  CAS  PubMed  Google Scholar 

  • Colcombet J, Boisson-Dernier A, Ros-Palau R, Vera CE, Schroeder JI (2005) Arabidopsis SOMATIC EMBRYOGENESIS RECEPTOR KINASES1 and 2 are essential for tapetum development and microspore maturation. Plant Cell 17:3350–3361

    Article  CAS  PubMed  Google Scholar 

  • Cooke R, Raynal M, Laudié M, Grellet F, Delseny M, Morris PC, Guerrier D, Giraudat J, Quigley F, Clabault G, Li YF, Mache R, Krivitzky M, Gy IJ, Kreis M, Lecharny A, Parmentier Y, Marbach J, Fleck J, Clément B, Philipps G, Hervé C, Bardet C, Tremousaygue D, Höfte H (1996) Further progress towards a catalogue of all Arabidopsis genes: analysis of a set of 5000 non-redundant ESTs. Plant J 9:101–124

    Article  CAS  PubMed  Google Scholar 

  • De Smet I, Voss U, Jürgens G, Beeckman T (2009) Receptor-like kinases shape the plant. Nat Cell Biol 11:1166–1173

    Article  PubMed  Google Scholar 

  • Debeaujon I, Leon-Kloosterziel KM, Koornneef M (2000) Influence of the testa on seed dormancy, germination, and longevity in Arabidopsis. Plant Physiol 122:403–414

    Article  CAS  PubMed  Google Scholar 

  • Dievart A, Clark SE (2004) LRR-containing receptors regulating plant development and defense. Development 131:251–261

    Article  CAS  PubMed  Google Scholar 

  • Edwards K, Johnstone C, Thompson C (1991) A simple and rapid method for the preparation of plant genomic DNA for PCR analysis. Nucleic Acids Res 19:1349

    Article  CAS  PubMed  Google Scholar 

  • Finch-Savage WE, Leubner-Metzger G (2006) Seed dormancy and the control of germination. New Phytol 171:501–523

    Article  CAS  PubMed  Google Scholar 

  • Holdsworth MJ, Bentsink L, Soppe WJ (2008) Molecular networks regulating Arabidopsis seed maturation, after-ripening, dormancy and germination. New Phytol 179:33–54

    Article  CAS  PubMed  Google Scholar 

  • Hord CL, Chen C, Deyoung BJ, Clark SE, Ma H (2006) The BAM1/BAM2 receptor-like kinases are important regulators of Arabidopsis early anther development. Plant Cell 18:1667–1680

    Article  CAS  PubMed  Google Scholar 

  • Kemp BP, Doughty J (2003) Just how complex is the Brassica S-receptor complex? J Exp Bot 54:157–168

    Article  CAS  PubMed  Google Scholar 

  • Kroj T, Savino G, Valon C, Giraudat J, Parcy F (2003) Regulation of storage protein gene expression in Arabidopsis. Development 130:6065–6073

    Article  CAS  PubMed  Google Scholar 

  • Lagarde D, Basset M, Lepetit M, Conejero G, Gaymard F, Astruc S, Grignon C (1996) Tissue-specific expression of Arabidopsis AKT1 gene is consistent with a role in K+ nutrition. Plant J 9:195–203

    Article  CAS  PubMed  Google Scholar 

  • Lefevre T, Thomas F, Schwartz A, Levashina E, Blandin S, Brizard JP, Le Bourligu L, Demettre E, Renaud F, Biron DG (2007) Malaria Plasmodium agent induces alteration in the head proteome of their Anopheles mosquito host. Proteomics 7:1908–1915

    Article  CAS  PubMed  Google Scholar 

  • Lopez-Molina L, Mongrand S, Chua NH (2001) A postgermination developmental arrest checkpoint is mediated by abscisic acid and requires the ABI5 transcription factor in Arabidopsis. Proc Natl Acad Sci USA 98:4782–4787

    Article  CAS  PubMed  Google Scholar 

  • Mittler R, Vanderauwera S, Gollery M, Van Breusegem F (2004) Reactive oxygen gene network of plants. Trends Plant Sci 9:490–498

    Article  CAS  PubMed  Google Scholar 

  • Morillo SA, Tax FE (2006) Functional analysis of receptor-like kinases in monocots and dicots. Curr Opin Plant Biol 9:460–469

    Article  CAS  PubMed  Google Scholar 

  • Muller K, Linkies A, Vreeburg RA, Fry SC, Krieger-Liszkay A, Leubner-Metzger G (2009) In vivo cell wall loosening by hydroxyl radicals during cress seed germination and elongation growth. Plant Physiol 150:1855–1865

    Article  PubMed  Google Scholar 

  • Nambara E, Keith K, McCourt P, Naito S (1994) Isolation of an internal deletion mutant of the Arabidopsis thaliana ABI3 gene. Plant Cell Physiol 35:509–513

    CAS  PubMed  Google Scholar 

  • Oracz K, Bouteau HE-M, Farrant JM, Cooper K, Belghazi M, Job C, Job D, Corbineau F, Bailly C (2007) ROS production and protein oxidation as a novel mechanism for seed dormancy alleviation. Plant J 50:452–465

    Article  CAS  PubMed  Google Scholar 

  • Oracz K, El-Maarouf-Bouteau H, Kranner I, Bogatek R, Corbineau F, Bailly C (2009) The mechanisms involved in seed dormancy alleviation by hydrogen cyanide unravel the role of reactive oxygen species as key factors of cellular signaling during germination. Plant Physiol 150:494–505

    Article  CAS  PubMed  Google Scholar 

  • Penfield S, King J (2009) Towards a systems biology approach to understanding seed dormancy and germination. Proc Biol Sci 276:3561–3569

    Article  CAS  PubMed  Google Scholar 

  • Penfield S, Li Y, Gilday AD, Graham S, Graham IA (2006) Arabidopsis ABA INSENSITIVE4 regulates lipid mobilization in the embryo and reveals repression of seed germination by the endosperm. Plant Cell 18:1887–1899

    Article  CAS  PubMed  Google Scholar 

  • Rajjou L, Gallardo K, Debeaujon I, Vandekerckhove J, Job C, Job D (2004) The effect of alpha-amanitin on the Arabidopsis seed proteome highlights the distinct roles of stored and neosynthesized mRNAs during germination. Plant Physiol 134:1598–1613

    Article  CAS  PubMed  Google Scholar 

  • Raz V, Bergervoet JH, Koornneef M (2001) Sequential steps for developmental arrest in Arabidopsis seeds. Development 128:243–252

    CAS  PubMed  Google Scholar 

  • Shiu SH, Bleecker AB (2001a) Plant receptor-like kinase gene family: diversity, function, and signaling. Sci STKE 2001:RE22

  • Shiu SH, Bleecker AB (2001b) Receptor-like kinases from Arabidopsis form a monophyletic gene family related to animal receptor kinases. Proc Natl Acad Sci USA 98:10763–10768

    Article  CAS  PubMed  Google Scholar 

  • Shiu SH, Bleecker AB (2003) Expansion of the receptor-like kinase/Pelle gene family and receptor-like proteins in Arabidopsis. Plant Physiol 132:530–543

    Article  CAS  PubMed  Google Scholar 

  • Shiu SH, Karlowski WM, Pan R, Tzeng YH, Mayer KF, Li WH (2004) Comparative analysis of the receptor-like kinase family in Arabidopsis and rice. Plant Cell 16:1220–1234

    Article  CAS  PubMed  Google Scholar 

  • Shpak ED, Lakeman MB, Torii KU (2003) Dominant-negative receptor uncovers redundancy in the Arabidopsis ERECTA leucine-rich repeat receptor-like kinase signaling pathway that regulates organ shape. Plant Cell 15:1095–1110

    Article  CAS  PubMed  Google Scholar 

  • Stenvik GE, Tandstad NM, Guo Y, Shi CL, Kristiansen W, Holmgren A, Clark SE, Aalen RB, Butenko MA (2008) The EPIP peptide of INFLORESCENCE DEFICIENT IN ABSCISSION is sufficient to induce abscission in Arabidopsis through the receptor-like kinases HAESA and HAESA-LIKE2. Plant Cell 20:1805–1817

    Article  CAS  PubMed  Google Scholar 

  • Tichtinsky G, Vanoosthuyse V, Cock JM, Gaude T (2003) Making inroads into plant receptor kinase signalling pathways. Trends Plant Sci 8:231–237

    Article  CAS  PubMed  Google Scholar 

  • To A, Valon C, Savino G, Guilleminot J, Devic M, Giraudat J, Parcy F (2006) A network of local and redundant gene regulation governs Arabidopsis seed maturation. Plant Cell 18:1642–1651

    Article  CAS  PubMed  Google Scholar 

  • Tör M, Lotze MT, Holton N (2009) Receptor-mediated signalling in plants: molecular patterns and programmes. J Exp Bot 60:3645–3654

    Article  PubMed  Google Scholar 

  • Torii KU (2004) Leucine-rich repeat receptor kinases in plants: structure, function, and signal transduction pathways. Int Rev Cytol 234:1–46

    Article  CAS  PubMed  Google Scholar 

  • Tsuwamoto R, Fukuoka H, Takahata Y (2008) GASSHO1 and GASSHO2 encoding a putative leucine-rich repeat transmembrane-type receptor kinase are essential for the normal development of the epidermal surface in Arabidopsis embryos. Plant J 54:30–42

    Article  CAS  PubMed  Google Scholar 

  • Vicient CM, Delseny M (1999) Isolation of total RNA from Arabidopsis thaliana seeds. Anal Biochem 268:412–413

    Article  CAS  PubMed  Google Scholar 

  • Vicient CM, Hull G, Guilleminot J, Devic M, Delseny M (2000) Differential expression of the Arabidopsis genes coding for Em-like proteins. J Exp Bot 51:1211–1220

    Article  CAS  PubMed  Google Scholar 

  • Wang H, Chevalier D, Larue C, Cho SK, Walker JC (2007) The protein phosphatases and protein kinases of Arabidopsis thaliana. In: Last R, Chang C, Jander G, Kliebenstein D, McClung R, Millar H (eds) The Arabidopsis book. The American Society of Plant Biologists, Rockville, MD, pp 1–38

    Google Scholar 

  • West M, Yee KM, Danao J, Zimmerman JL, Fischer RL, Goldberg RB, Harada JJ (1994) LEAFY COTYLEDON1 is an essential regulator of late embryogenesis and cotyledon identity in Arabidopsis. Plant Cell 6:1731–1745

    Article  CAS  PubMed  Google Scholar 

  • Yin Y, Wu D, Chory J (2002) Plant receptor kinases: systemin receptor identified. Proc Natl Acad Sci USA 99:9090–9092

    Article  CAS  PubMed  Google Scholar 

  • Zimmermann P, Hennig L, Gruissem W (2005) Gene-expression analysis and network discovery using Genevestigator. Trends Plant Sci 10:407–409

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

We thank F. Parcy (CNRS, CEA Grenoble, France) for the gift of abi3-6 seeds, M. Devic (CNRS, IRD Montpellier, France) for the gift of lec1-2 seeds and N. Bies-Etheve (UPVD, Perpignan, France) for the abi5-5 mutant. We are grateful to J.P. Brizard (IRD Montpellier, France) for 2-D DIGE analysis and the proteomics platform of Montpellier Genopole for MS analysis. We finally wish to thank two anonymous reviewers for their helpful comments. Financial support was provided by the Centre National de la Recherche Scientifique (CNRS). D.P. was supported by a scholarship from the French Ministry of Research and Education.

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Pitorre, D., Llauro, C., Jobet, E. et al. RLK7, a leucine-rich repeat receptor-like kinase, is required for proper germination speed and tolerance to oxidative stress in Arabidopsis thaliana . Planta 232, 1339–1353 (2010). https://doi.org/10.1007/s00425-010-1260-4

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